Comparative genomic analysis of symbiotic and free-living strains provides insights into the evolutionary origins of obligate -bacterial endosymbioses.

UNLABELLED

Endosymbiosis is a widespread and important phenomenon requiring diverse model systems. Ciliates are a widespread group of protists that often form symbioses with diverse microorganisms. Endosymbioses between the ciliate and heritable bacterial symbionts are common in nature, and four essential symbionts were described: , " Protistobacter heckmanni," ". Devosia symbiotica," and ". Devosia euplotis." Among them, only the genus comprises very close free-living and symbiotic representatives, which makes it an excellent model for investigating symbiont replacements and recent symbioses. In this article, we characterized a novel endosymbiont inhabiting the cytoplasm of and found that it is a close relative of the free-living bacterium ( and ). We present the complete genome sequence and annotation of the symbiotic . Comparative analyses indicate that the genome of symbiotic is small in size and rich in pseudogenes when compared with free-living strains, which seems to fit the prediction for recently established endosymbionts undergoing genome erosion. Further comparative analysis revealed reduced metabolic capacities in symbiotic , which implies that the symbiont relies on the host for carbon sources, organic nitrogen and sulfur, and some cofactors. We also estimated substitution rates between symbiotic and free-living pairs for 233 genes; the results showed that symbiotic displays higher dN/dS mean value than free-living relatives, which suggested that genetic drift is the main driving force behind molecular evolution in endosymbionts.

IMPORTANCE

In the long history of symbiosis research, most studies focused mainly on organelles or bacteria within multicellular hosts. The single-celled protists receive little attention despite harboring an immense diversity of symbiotic associations with bacteria and archaea. One subgroup of the ciliate species is strictly dependent on essential symbionts for survival and has emerged as a valuable model for understanding symbiont replacements and recent symbioses. However, almost all of our knowledge about the evolution and functions of symbioses comes from the - system. In this article, we report a novel essential symbiont, which also has very close free-living relatives. Genome analysis indicated that it is a recently established endosymbiont undergoing genome erosion and relies on the host for many essential molecules. Our results provide support for the notion that essential symbionts of the ciliate evolve from free-living progenitors in the natural water environment.